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Reduced tolerance to simulated herbivory on clonal organs in alien genotypes: a multi-species experiment with native and introduced origins

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Abstract

Clonal growth may increase the likelihood for alien plants becoming invasive, as it is an efficient foraging and spatial exploration strategy. Here, we investigated the effect of artificial herbivory on organs of clonal growth and its potential to drive post-introduction evolutionary change. Based on the assumption that tolerance traits are costly and that clonal alien species may benefit from investing freed resources into growth, fecundity or nutrient acquisition, we tested the hypothesis of lower tolerance to herbivory on organs of clonal growth in alien plants. In a common-garden experiment we studied divergence in plants from native German and alien New Zealand populations of six species with different clonal growth forms. A nutrient treatment testing the plant’s acquisition abilities, was combined with artificial herbivory on clonal organs. We investigated origin-dependent differences in sexual reproduction, plant growth and the production of clonal organs. For aboveground and clonal organ biomass, alien plants showed lower tolerance to artificial herbivory on clonal organs than native plants. In the combined herbivory and nutrient treatment, alien plants of four species grew fewer clonal organs when compared to the nutrient treatment alone. Alien plants of the other two species produced more clonal organs, regardless of treatment. All species revealed significant differences in flower production between origins, with five of them producing more flowers on alien than on native plants. The results support the hypothesis that a release of herbivory on clonal organs has lead to subtle evolutionary changes in tolerance of alien plants and to a species-dependent increase in plant vigour, clonal growth and/or sexual reproduction that may enhance their invasive success.

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References

  • Agrawal AA, Hastings AP, Johnson MT, Maron JL, Salminen J-P (2012) Insect herbivores drive real-time ecological and evolutionary change in plant populations. Science 338:113–116

    Article  CAS  PubMed  Google Scholar 

  • Alpert P (1996) Nutrient sharing in natural clonal fragments of Fragaria chiloensis. J Ecol 84:395–406

    Article  Google Scholar 

  • Alpert P (1999) Effects of clonal integration on plant plasticity in Fragaria chiloensis. Plant Ecol 141:99–106

    Article  Google Scholar 

  • Atwood J, Meyerson L (2011) Beyond EICA: understanding post-establishment evolution requires a broader evaluation of potential selection pressures. NeoBiota 10:7–25

    Article  Google Scholar 

  • Baker HG (1974) The evolution of weeds. Annu Rev Ecol Evol Syst 5:1–24

    Article  Google Scholar 

  • Baldwin IT (1998) Jasmonate-induced responses are costly but benefit plants under attack in native populations. Proc Natl Acad Sci USA 95:8113

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Barney JN, Whitlow TH, DiTommaso A (2009) Evolution of an invasive phenotype: shift to belowground dominance and enhanced competitive ability in the introduced range. Plant Ecol 202:275–284

    Article  Google Scholar 

  • Baruch Z, Gómez JA (1996) Dynamics of energy and nutrient concentration and construction cost in a native and two alien C 4 grasses from two neotropical savannas. Plant Soil 181:175–184

    Article  CAS  Google Scholar 

  • Bastlova D, Kvet J (2002) Differences in dry weight partitioning and flowering phenology between native and non-native plants of purple loosestrife (Lythrum salicaria L.). Flora 197:332–340

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker B (2012) lme4: linear mixed-effects models using S4 classes

  • Bazzaz FA, Chiariello NR, Coley PD, Pitelka LF (1987) Allocating resources to reproduction and defense. Bioscience 37:58–67

    Article  Google Scholar 

  • Beckmann M, Erfmeier A, Bruelheide H (2009) A comparison of native and invasive populations of three clonal plant species in Germany and New Zealand. J Biogeogr 36:865–878

    Article  Google Scholar 

  • Beckmann M, Hock M, Bruelheide H, Erfmeier A (2012) The role of UV-B radiation in the invasion of Hieracium pilosella—a comparison of German and New Zealand plants. Environ Exp Bot 75:173–180

    Article  Google Scholar 

  • Beckmann M, Bruelheide H, Erfmeier A (2014) Local performance of six clonal alien species differs between native and invasive regions in Germany and New Zealand. Austral Ecol 39:378–387

    Article  Google Scholar 

  • Bishop GF, Davy AJ (1994) Hieracium pilosella L. (Pilosella officinarum F. Schultz & Schultz-Bip.). J Ecol 82:195–210

    Article  Google Scholar 

  • Blossey B, Notzold R (1995) Evolution of increased competitive ability in invasive nonindigenous plants: a hypothesis. J Ecol 83:887–889

    Article  Google Scholar 

  • Blumenthal DM, Hufbauer RA (2007) Increased plant size in exotic populations: a common-garden test with 14 invasive species. Ecology 88:2758–2765

    Article  PubMed  Google Scholar 

  • Bossdorf O, Lipowsky A, Prati D (2008) Selection of preadapted populations allowed Senecio inaequidens to invade Central Europe. Divers Distrib 14:676–685

    Article  Google Scholar 

  • Brown JS, Eckert CG (2005) Evolutionary increase in sexual and clonal reproductive capacity during biological invasion in an aquatic plant Butomus umbellatus (Butomaceae). Am J Bot 92:495–502

    Article  PubMed  Google Scholar 

  • Buschmann H, Edwards P, Dietz H (2005) Variation in growth pattern and response to slug damage among native and invasive provenances of four perennial Brassicaceae species. J Ecol 93:322–334

    Article  Google Scholar 

  • Buschmann H, Edwards PJ, Dietz H (2006) Responses of native and invasive Brassicaceae species to slug herbivory. Acta Oecol Int J Ecol 30:126–135

    Article  Google Scholar 

  • Carrillo J, McDermott D, Siemann E (2014) Loss of specificity: native but not invasive populations of Triadica sebifera vary in tolerance to different herbivores. Oecologia 174:863–871

    Article  PubMed  Google Scholar 

  • Catford JA, Jansson R, Nilsson C (2009) Reducing redundancy in invasion ecology by integrating hypotheses into a single theoretical framework. Divers Distrib 15:22–40

    Article  Google Scholar 

  • Chun YJ (2011) Phenotypic plasticity of introduced versus native purple loosestrife: univariate and multivariate reaction norm approaches. Biol Invasions 13:819–829

    Article  Google Scholar 

  • Daws MI, Hall J, Flynn S, Pritchard HW (2007) Do invasive species have bigger seeds? evidence from intra- and inter-specific comparisons. S Afr J Bot 73:138–143

    Article  Google Scholar 

  • de Kroon H, Hutchings MJ (1995) Morphological plasticity in clonal plants: the foraging concept reconsidered. J Ecol 83:143–152

    Article  Google Scholar 

  • de Kroon H, van Groenendael J (1997) The ecology and evolution of clonal plants. Backhuys Publishers, Leiden

    Google Scholar 

  • Ebeling SK, Stöcklin J, Hensen I, Auge H (2011) Multiple common garden experiments suggest lack of local adaptation in an invasive ornamental plant. J Plant Ecol 4:209–220

    Article  Google Scholar 

  • Erfmeier A (2013) Constraints and release at different scales—the role of adaptation in biological invasions. Basic Appl Ecol 14:281–288

    Article  Google Scholar 

  • Erfmeier A, Bruelheide H (2004) Comparison of native and invasive Rhododendron ponticum populations: growth, reproduction and morphology under field conditions. Flora 199:120–133

    Article  Google Scholar 

  • Fenner M, Lee WG (2001) Lack of pre-dispersal seed predators in introduced Asteraceae in New Zealand. N Z J Ecol 25:95–99

    Google Scholar 

  • Fornoni J (2011) Ecological and evolutionary implications of plant tolerance to herbivory. Funct Ecol 25:399–407

    Article  Google Scholar 

  • Givnish TJ (2002) Ecological constraints on the evolution of plasticity in plants. Evol Ecol 16:213–242

    Article  Google Scholar 

  • He M, Ding J, Lu X (2014) Increased compensatory ability of an invasive plant to above- and below-ground enemies in monocultures. Plant Ecol 215:253–260

    Article  Google Scholar 

  • Howell C (2008) Consolidated list of environmental weeds in New Zealand: weeds. Available from http://doc.govt.nz/publications/conservation/threats-and-impacts/weeds/consolidated-list-of-environmental-weeds-in-new-zealand/. Accessed Feb 2011

  • Huang W, Siemann E, Wheeler GS, Zou J, Carrillo J, Ding J (2010) Resource allocation to defence and growth are driven by different responses to generalist and specialist herbivory in an invasive plant. J Ecol 98:1157–1167

    Article  Google Scholar 

  • Hull-Sanders HM, Clare R, Johnson RH, Meyer GA (2007) Evaluation of the evolution of increased competitive ability (EICA) hypothesis: loss of defense against generalist but not specialist herbivores. J Chem Ecol 33:781–799

    Article  CAS  PubMed  Google Scholar 

  • Jakobs G, Weber E, Edwards PJ (2004) Introduced plants of the invasive Solidago gigantea (Asteraceae) are larger and grow denser than conspecifics in the native range. Divers Distrib 10:11–19

    Article  Google Scholar 

  • Joshi S, Tielbörger K (2012) Response to enemies in the invasive plant Lythrum salicaria is genetically determined. Ann Bot 110:1403–1410

    Article  PubMed Central  PubMed  Google Scholar 

  • Joshi J, Vrieling K (2005) The enemy release and EICA hypothesis revisited: incorporating the fundamental difference between specialist and generalist herbivores. Ecol Lett 8:704–714

    Article  Google Scholar 

  • Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170

    Article  Google Scholar 

  • Klimeš L, Klimešova J, Hendriks R (1997) Clonal plant architecture: a comparative analysis of form and function. In: De Kroon H, Van Groenendael JM (eds) The ecology and evolution of clonal plants. Backhuys Publishers, Leiden, pp 1–29

    Google Scholar 

  • Klimešová J, de Bello F (2009) CLO-PLA: the database of clonal and bud bank traits of Central European flora. J Veg Sci 20:511–516

    Article  Google Scholar 

  • Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. Trends Ecol Evol 16:199–204

    Article  PubMed  Google Scholar 

  • Kuznetsova A, Brockhoff PB (2012) MixMod: analysis of mixed models. R package version 1.0

  • Lankau RA (2007) Specialist and generalist herbivores exert opposing selection on a chemical defense. New Phytol 175:176–184

    Article  PubMed  Google Scholar 

  • Liu H, Stiling P (2006) Testing the enemy release hypothesis: a review and meta-analysis. Biol Invasions 8:1535–1545

    Article  Google Scholar 

  • Liu J, Dong M, Miao SL, Li Z, Song MH, Wang RQ (2006) Invasive alien plants in China: role of clonality and geographical origin. Biol Invasions 8:1461–1470

    Article  Google Scholar 

  • Lowett Doust L (1981) Population dynamics and local specialization in a clonal perennial (Ranunculus repens): I. The dynamics of ramets in contrasting habitats. J Ecol 69:743–755

    Article  Google Scholar 

  • Maron JL, Vilà M, Bommarco R, Elmendorf S, Beardsley P (2004) Rapid evolution of an invasive plant. Ecol Monogr 74:261–280

    Article  Google Scholar 

  • McKey D, Elias M, Pujol B, Duputié A (2010) The evolutionary ecology of clonally propagated domesticated plants. New Phytol 186:318–332

    Article  PubMed  Google Scholar 

  • Meyer G, Hull-Sanders H (2008) Altered patterns of growth, physiology and reproduction in invasive genotypes of Solidago gigantea (Asteraceae). Biol Invasions 10:303–317

    Article  Google Scholar 

  • Meyer G, Clare R, Weber E (2005) An experimental test of the evolution of increased competitive ability hypothesis in goldenrod, Solidago gigantea. Oecologia 144:299–307

    Article  PubMed  Google Scholar 

  • Montague JL, Barrett SCH, Eckert CG (2008) Re-establishment of clinal variation in flowering time among introduced populations of purple loosestrife (Lythrum salicaria, Lythraceae). J Evol Biol 21:234–245

    CAS  PubMed  Google Scholar 

  • Morrison JA, Mauck K (2007) Experimental field comparison of native and non-native maple seedlings: natural enemies, ecophysiology, growth and survival. J Ecol 95:1036–1049

    Article  Google Scholar 

  • Oduor AMO, Lankau RA, Strauss SY, Gómez JM (2011) Introduced Brassica nigra populations exhibit greater growth and herbivore resistance but less tolerance than native populations in the native range. New Phytol 191:536–544

    Article  PubMed  Google Scholar 

  • Otfinowski R, Kenkel NC (2008) Clonal integration facilitates the proliferation of smooth brome clones invading northern fescue prairies. Plant Ecol 199:235–242

    Article  Google Scholar 

  • Pan JJ, Price JS (2001) Fitness and evolution in clonal plants: the impact of clonal growth. Evol Ecol 15:583–600

    Article  Google Scholar 

  • Peltzer DA (2002) Does clonal integration improve competitive ability? A test using aspen (Populus tremuloides [Salicaceae]) invasion into prairie. Am J Bot 89:494–499

    Article  PubMed  Google Scholar 

  • Perglova I, Pergl J, Moravcova L (2009) Differences in germination and seedling establishment of alien and native Impatiens species. Preslia 81:357–375

    Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D, R Development Core Team (2011) nlme: linear and nonlinear mixed effects models. R package version, 3, 103.

  • Rejmánek M, Richardson DM (1996) What attributes make some plant species more invasive? Ecology 77:1655–1661

    Article  Google Scholar 

  • Rothmaler W, Jäger EJ, Werner K (2005) Exkursionsflora von Deutschland 4: Gefäßpflanzen: Kritischer Band: Bd. 4, 10. A. Spektrum Akademischer Verlag

  • Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Baughman S, Cabin RJ, Cohen JE, Ellstrand NC et al (2001) The population biology of invasive species. Annu Rev Ecol Evol Syst 32:305–332

    Article  Google Scholar 

  • Scheidel U, Röhl S, Bruelheide H (2003) Altitudinal gradients of generalist and specialist herbivory on three montane Asteraceae. Acta Oecol Int J Ecol 24:275–283

    Article  Google Scholar 

  • Stastny M, Schaffner U, Elle E (2005) Do vigour of introduced populations and escape from specialist herbivores contribute to invasiveness? J Ecol 93:27–37

    Article  Google Scholar 

  • Strauss SY, Agrawal AA (1999) The ecology and evolution of plant tolerance to herbivory. Trends Ecol Evol 14:179–185

    Article  PubMed  Google Scholar 

  • Thébaud C, Simberloff D (2001) Are plants really larger in their introduced ranges? Am Nat 157:231–236

    Article  PubMed  Google Scholar 

  • Theoharides KA, Dukes JS (2007) Plant invasion across space and time: factors affecting nonindigenous species success during four stages of invasion. New Phytol 176:256–273

    Article  PubMed  Google Scholar 

  • Thorpe AS, Thelen GC, Diaconu A, Callaway RM (2009) Root exudate is allelopathic in invaded community but not in native community: field evidence for the novel weapons hypothesis. J Ecol 97:641–645

    Article  Google Scholar 

  • van Kleunen M, Schmid B (2003) No evidence for an evolutionary increased competitive ability in an invasive plant. Ecology 84:2816–2823

    Article  Google Scholar 

  • van Kleunen M, Fischer M, Schmid B (2000) Clonal integration in Ranunculus reptans: by-product or adaptation? J Evol Biol 13:237–248

    Article  Google Scholar 

  • Wang N, Yu FH, Li PX, He WM, Liu FH, Liu JM, Dong M (2008) Clonal integration affects growth, photosynthetic efficiency and biomass allocation, but not the competitive ability, of the alien invasive Alternanthera philoxeroides under severe stress. Ann Bot 101:671

    Article  PubMed Central  PubMed  Google Scholar 

  • Webb CJ, Sykes WR, Garnock-Jones PJ (1988) Flora of New Zealand volume IV: naturalised pteridophytes, gymnosperms, dicotyledons. Botany Division, Department of Scientific and Industrial Research, Wellington

  • Willis AJ, Memmott J, Forrester RI (2000) Is there evidence for the post-invasion evolution of increased size among invasive plant species? Ecol Lett 3:275–283

    Article  Google Scholar 

  • Woodburn TL, Sheppard AW (1996) The demography of Carduus nutans as a native and an alien weed. Plant Prot Q 11:236–238

    Google Scholar 

  • Yang X, Huang W, Tian B, Ding J (2014) Differences in growth and herbivory damage of native and invasive kudzu (Peuraria montana var. lobata) populations grown in the native range. Plant Ecol 215:339–346

    Article  Google Scholar 

  • Zou J, Siemann E, Rogers WE, DeWalt SJ (2008) Decreased resistance and increased tolerance to native herbivores of the invasive plant Sapium sebiferum. Ecography 31:663–671

    Article  Google Scholar 

  • Zuur AF, Ieno EN, Walker N, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R, 1st edn. Springer, Berlin

    Book  Google Scholar 

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Acknowledgments

The manuscript profited from valuable comments by three unknown reviewers. This study was supported financially by the German state of Saxony-Anhalt (Landesgraduiertenförderung) as part of the Ph.D. project of M. B. We thank S. Rogahn, C. Rosche, M. Hock, A. Zeuner, S. Pflug, E. Bremer and C. Voigt for their help in setting up and maintenance of the experiment and harvesting the plants. Seed collection was possible due to a travel Grant for M.B. from the German Academic Exchange Service (DAAD). Mary Korver from Manaaki Whenua Landcare Research Institute is thanked for shipping assistance.

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Correspondence to Michael Beckmann.

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Beckmann, M., Bruelheide, H. & Erfmeier, A. Reduced tolerance to simulated herbivory on clonal organs in alien genotypes: a multi-species experiment with native and introduced origins. Biol Invasions 18, 549–563 (2016). https://doi.org/10.1007/s10530-015-1027-8

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